Extracellular superoxide dismutase VdSOD5 is required for virulence in Verticillium dahliae

Plants produce reactive oxygen species (ROS) to defend pathogens. To counteract this attack, certain pathogens express superoxide dismutases (SODs) to scavenge host-derived ROS. However, the roles of SODs in Verticillium dahliae, an important vascular pathogen, are not clear. Our previous study has...

Full description

Bibliographic Details
Main Authors: Li TIAN, Cai-min HUANG, Dan-dan ZHANG, Ran LI, Jie-yin CHEN, Wei-xia SUN, Nian-wei QIU, Xiao-feng DAI
Format: Article
Language:English
Published: Elsevier 2021-07-01
Series:Journal of Integrative Agriculture
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2095311920633536
_version_ 1829490255688892416
author Li TIAN
Cai-min HUANG
Dan-dan ZHANG
Ran LI
Jie-yin CHEN
Wei-xia SUN
Nian-wei QIU
Xiao-feng DAI
author_facet Li TIAN
Cai-min HUANG
Dan-dan ZHANG
Ran LI
Jie-yin CHEN
Wei-xia SUN
Nian-wei QIU
Xiao-feng DAI
author_sort Li TIAN
collection DOAJ
description Plants produce reactive oxygen species (ROS) to defend pathogens. To counteract this attack, certain pathogens express superoxide dismutases (SODs) to scavenge host-derived ROS. However, the roles of SODs in Verticillium dahliae, an important vascular pathogen, are not clear. Our previous study has shown that a putative extracellular SOD (VdSOD5) of V. dahliae is significantly induced by culturing in cotton tissues, suggesting that VdSOD5 may play an important role in host–pathogen interactions and virulence. Here, we showed that VdSOD5 encoded a superoxide dismutase with a cofactor copper-binding site and a functional signal peptide that can conduct protein secretion in an invertase-mutated yeast strain. The mutations in VdSOD5 (ΔVdSOD5) did not change the normal vegetative growth and conidial production but reduced the virulence of V. dahliae on susceptible host cotton. Further studies showed that the transcription of VdSOD5 was significantly up-regulated during the early stage of infection, and the loss-of-function of VdSOD5 decreased culture filtrate and fungal tissue SOD activities of V. dahliae by 74 and 28%, respectively. Compared to the wild-type strain Vd991, the ΔVdSOD5 showed the same sensitivity to the intracellular ROS generator menadione. Furthermore, nitroblue tetrazolium (NBT) staining demonstrated that VdSOD5 functioned in the detoxification of superoxides generated by host roots during infection. These results suggest that VdSOD5 of V. dahliae is an important virulence factor, secreted out of cells to combat host-derived ROS.
first_indexed 2024-12-15T00:21:22Z
format Article
id doaj.art-c50d83ddbf23495c8d51402c95d3dc1f
institution Directory Open Access Journal
issn 2095-3119
language English
last_indexed 2024-12-15T00:21:22Z
publishDate 2021-07-01
publisher Elsevier
record_format Article
series Journal of Integrative Agriculture
spelling doaj.art-c50d83ddbf23495c8d51402c95d3dc1f2022-12-21T22:42:18ZengElsevierJournal of Integrative Agriculture2095-31192021-07-0120718581870Extracellular superoxide dismutase VdSOD5 is required for virulence in Verticillium dahliaeLi TIAN0Cai-min HUANG1Dan-dan ZHANG2Ran LI3Jie-yin CHEN4Wei-xia SUN5Nian-wei QIU6Xiao-feng DAI7College of Life Science, Qufu Normal University, Qufu 273165, P.R.ChinaCollege of Life Science, Qufu Normal University, Qufu 273165, P.R.ChinaState Key Laboratory for Biology of Plant Diseases and Insect Pests/Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, P.R.ChinaState Key Laboratory for Biology of Plant Diseases and Insect Pests/Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, P.R.ChinaState Key Laboratory for Biology of Plant Diseases and Insect Pests/Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, P.R.ChinaCollege of Life Science, Qufu Normal University, Qufu 273165, P.R.ChinaCollege of Life Science, Qufu Normal University, Qufu 273165, P.R.China; Correspondence QIU Nian-wei, Tel: +86-537-4456415State Key Laboratory for Biology of Plant Diseases and Insect Pests/Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, P.R.China; Correspondence DAI Xiao-feng, Tel: +86-10-62813566Plants produce reactive oxygen species (ROS) to defend pathogens. To counteract this attack, certain pathogens express superoxide dismutases (SODs) to scavenge host-derived ROS. However, the roles of SODs in Verticillium dahliae, an important vascular pathogen, are not clear. Our previous study has shown that a putative extracellular SOD (VdSOD5) of V. dahliae is significantly induced by culturing in cotton tissues, suggesting that VdSOD5 may play an important role in host–pathogen interactions and virulence. Here, we showed that VdSOD5 encoded a superoxide dismutase with a cofactor copper-binding site and a functional signal peptide that can conduct protein secretion in an invertase-mutated yeast strain. The mutations in VdSOD5 (ΔVdSOD5) did not change the normal vegetative growth and conidial production but reduced the virulence of V. dahliae on susceptible host cotton. Further studies showed that the transcription of VdSOD5 was significantly up-regulated during the early stage of infection, and the loss-of-function of VdSOD5 decreased culture filtrate and fungal tissue SOD activities of V. dahliae by 74 and 28%, respectively. Compared to the wild-type strain Vd991, the ΔVdSOD5 showed the same sensitivity to the intracellular ROS generator menadione. Furthermore, nitroblue tetrazolium (NBT) staining demonstrated that VdSOD5 functioned in the detoxification of superoxides generated by host roots during infection. These results suggest that VdSOD5 of V. dahliae is an important virulence factor, secreted out of cells to combat host-derived ROS.http://www.sciencedirect.com/science/article/pii/S2095311920633536Verticillium dahliaesuperoxide dismutasesecretionvirulenceROS detoxification
spellingShingle Li TIAN
Cai-min HUANG
Dan-dan ZHANG
Ran LI
Jie-yin CHEN
Wei-xia SUN
Nian-wei QIU
Xiao-feng DAI
Extracellular superoxide dismutase VdSOD5 is required for virulence in Verticillium dahliae
Journal of Integrative Agriculture
Verticillium dahliae
superoxide dismutase
secretion
virulence
ROS detoxification
title Extracellular superoxide dismutase VdSOD5 is required for virulence in Verticillium dahliae
title_full Extracellular superoxide dismutase VdSOD5 is required for virulence in Verticillium dahliae
title_fullStr Extracellular superoxide dismutase VdSOD5 is required for virulence in Verticillium dahliae
title_full_unstemmed Extracellular superoxide dismutase VdSOD5 is required for virulence in Verticillium dahliae
title_short Extracellular superoxide dismutase VdSOD5 is required for virulence in Verticillium dahliae
title_sort extracellular superoxide dismutase vdsod5 is required for virulence in verticillium dahliae
topic Verticillium dahliae
superoxide dismutase
secretion
virulence
ROS detoxification
url http://www.sciencedirect.com/science/article/pii/S2095311920633536
work_keys_str_mv AT litian extracellularsuperoxidedismutasevdsod5isrequiredforvirulenceinverticilliumdahliae
AT caiminhuang extracellularsuperoxidedismutasevdsod5isrequiredforvirulenceinverticilliumdahliae
AT dandanzhang extracellularsuperoxidedismutasevdsod5isrequiredforvirulenceinverticilliumdahliae
AT ranli extracellularsuperoxidedismutasevdsod5isrequiredforvirulenceinverticilliumdahliae
AT jieyinchen extracellularsuperoxidedismutasevdsod5isrequiredforvirulenceinverticilliumdahliae
AT weixiasun extracellularsuperoxidedismutasevdsod5isrequiredforvirulenceinverticilliumdahliae
AT nianweiqiu extracellularsuperoxidedismutasevdsod5isrequiredforvirulenceinverticilliumdahliae
AT xiaofengdai extracellularsuperoxidedismutasevdsod5isrequiredforvirulenceinverticilliumdahliae